Dopamine Receptor Activation Modulates GABA Neuron Migration from the Basal Forebrain to the Cerebral Cortex
Open accessAbstract
GABA neurons of the cerebral cortex and other telencephalic structures are produced in the basal forebrain and migrate to their final destinations during the embryonic period. The embryonic basal forebrain is enriched in dopamine and its receptors, creating a favorable environment for dopamine to influence GABA neuron migration. However, whether dopamine receptor activation can influence GABA neuron migration is not known. We show that dopamine D 1 receptor activation promotes and D 2 receptor activation decreases GABA neuron migration from the medial and caudal ganglionic eminences to the cerebral cortex in slice preparations of embryonic mouse forebrain. Slice preparations from D 1 or D 2 receptor knock-out mouse embryos confirm the findings. In addition, D 1 receptor electroporation into cells of the basal forebrain and pharmacological activation of the receptor promote migration of the electroporated cells to the cerebral cortex. Analysis of GABA neuron numbers in the cerebral wall of the dopamine receptor knock-out mouse embryos further confirmed the effects of dopamine receptor activation on GABA neuron migration. Finally, dopamine receptor activation mobilizes striatal neuronal cytoskeleton in a manner consistent with the effects on neuronal migration. These data show that impairing the physiological balance between D 1 and D 2 receptors can alter GABA neuron migration from the basal forebrain to the cerebral cortex. The intimate relationship between dopamine and GABA neuron development revealed here may offer novel insights into developmental disorders such as schizophrenia, attention deficit or autism, and fetal cocaine exposure, all of which are associated with dopamine and GABA imbalance.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Dopamine and GABA interactions can influence proliferation, migration and synaptogenesis.
“It has furthermore been shown that dopamine and GABA interactions can influence these processes [187, 188].”
From Development of prefrontal cortex (2022) · cites this paper as [188]
The Discussion (page unavailable) reports that dopamine receptor activation affects GABA neuron migration and describes dopamine’s role in neuroepithelial-cell proliferation. The Introduction (page unavailable) says GABA neurons modulate proliferation and circuit formation, but the paper does not establish that dopamine–GABA interactions influence synaptogenesis. (LLM, conf=0.86)
Experimental — accuracy not yet measuredIn development, the balance of dopamine D1 and D2 receptor activation is critical for GABA neuron migration from basal forebrain to cerebral cortex and may contribute to developmental disorders such as autism.
“In development, the physiological balance of dopamine D1 and D2 receptor activation is critical for GABA neuron migration from the basal forebrain to the cerebral cortex and may contribute to developmental disorders such as autism [181].”
From Consensus Paper: Pathological Role of the Cerebellum in Autism (2012) · cites this paper as [181]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Shrestha, S., & Offer, S. M. (2016) · Medical Epigenetics · doi:10.1159/000444713 · Cited by 8,949 · see citing works
Efficient selection for high-expression transfectants with a novel eukaryotic vector
Niwa, H., Yamamura, K., & Miyazaki, J. (1991) · Gene · doi:10.1016/0378-1119(91)90434-d · Cited by 5,135 · see citing works
Noctor, S. C., Martínez-Cerdeño, V., Ivic, L., & Kriegstein, A. R. (2004) · Nature Neuroscience · doi:10.1038/nn1172 · Cited by 2,229 · see citing works
The Atlas of Mouse Development
Kaufman, M. H. (1992) · Medical Entomology and Zoology · Cited by 1,749 · see citing works
The neostriatal mosaic: multiple levels of compartmental organization
Gerfen, C. R. (1992) · Trends in Neurosciences · doi:10.1016/0166-2236(92)90355-c · Cited by 1,471 · see citing works
Interneuron Migration from Basal Forebrain to Neocortex: Dependence on <i>Dlx</i> Genes
Anderson, S. A., Eisenstat, D. D., Shi, L., & Rubenstein, J. L. R. (1997) · Science · doi:10.1126/science.278.5337.474 · Cited by 1,462 · see citing works
Is there more to gaba than synaptic inhibition?
Owens, D. F., & Kriegstein, A. R. (2002) · Nature reviews. Neuroscience · doi:10.1038/nrn919 · Cited by 1,158 · see citing works
A long, remarkable journey: Tangential migration in the telencephalon
Marín, Ó., & Rubenstein, J. L. R. (2001) · Nature reviews. Neuroscience · doi:10.1038/35097509 · Cited by 1,050 · see citing works
Molecular biology of dopamine receptors
Sibley, D. R., & Monsma, F. J. (1992) · Trends in Pharmacological Sciences · doi:10.1016/0165-6147(92)90025-2 · Cited by 993 · see citing works
Two dopamine receptors: Biochemistry, physiology and pharmacology
Stoof, J. C., & Kebabian, J. W. (1984) · Life Sciences · doi:10.1016/0024-3205(84)90519-8 · Cited by 942 · see citing works
GABAergic Mechanisms in Epilepsy
Treiman, D. M. (2001) · Epilepsia · doi:10.1046/j.1528-1157.2001.042suppl.3008.x · Cited by 836 · see citing works
Lavdas, A. A., Grigoriou, M., Pachnis, V., & Parnavelas, J. G. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-18-07881.1999 · Cited by 765 · see citing works
Coordinated Expression of Dopamine Receptors in Neostriatal Medium Spiny Neurons
Surmeier, D. J., Song, W., & Yan, Z. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-20-06579.1996 · Cited by 747 · see citing works
Wichterle, H., Turnbull, D. H., Nery, S., Fishell, G., & Alvarez-Buylla, A. (2001) · Development · doi:10.1242/dev.128.19.3759 · Cited by 722 · see citing works
Two modes of radial migration in early development of the cerebral cortex
Nadarajah, B., Brunstrom, J. E., Grutzendler, J., Wong, R., & Pearlman, A. L. (2001) · Nature Neuroscience · doi:10.1038/83967 · Cited by 689 · see citing works
Distinct cortical migrations from the medial and lateral ganglionic eminences
Anderson, S. A., Marín, Ó., Horn, C., Jennings, K., & Rubenstein, J. L. R. (2001) · Development · doi:10.1242/dev.128.3.353 · Cited by 651 · see citing works
Origins of Cortical Interneuron Subtypes
Xu, Q., Cobos, I., De La Cruz, E., Rubenstein, J. L., & Anderson, S. A. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.5667-03.2004 · Cited by 639 · see citing works
The temporal and spatial origins of cortical interneurons predict their physiological subtype
Butt, S. J. B., Fuccillo, M., Nery, S., Noctor, S., Kriegstein, A., Corbin, J. G., & Fishell, G. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.034 · Cited by 587 · see citing works
The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations
Nery, S., Fishell, G., & Corbin, J. G. (2002) · Nature Neuroscience · doi:10.1038/nn971 · Cited by 558 · see citing works
Theiler, K. (1972) · Cited by 550 · see citing works
Multipolar Migration: The Third Mode of Radial Neuronal Migration in the Developing Cerebral Cortex
Tabata, H., & Nakajima, K. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-31-09996.2003 · Cited by 541 · see citing works
Emerging principles of altered neural circuitry in schizophrenia
Benes, F. (2000) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00041-7 · Cited by 513 · see citing works
Young neurons from medial ganglionic eminence disperse in adult and embryonic brain
Wichterle, H., Garcia-Verdugo, J. M., Herrera, D. G., & Alvarez-Buylla, A. (1999) · Nature Neuroscience · doi:10.1038/8131 · Cited by 506 · see citing works
A LIS1/NUDEL/Cytoplasmic Dynein Heavy Chain Complex in the Developing and Adult Nervous System
Sasaki, S., Shionoya, A., Ishida, M., Gambello, M. J., Yingling, J., Wynshaw-Boris, A. J., & Hirotsune, S. (2000) · Neuron · doi:10.1016/s0896-6273(00)00146-x · Cited by 499 · see citing works
Short- and long-range attraction of cortical GABAergic interneurons by neuregulin-1
Flames, N., Long, J. E., Garratt, A. N., Fischer, T. M., Gassmann, M., Birchmeier, C., Lai, C., Rubenstein, J. L. R., & Marı́n, O. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.028 · Cited by 431 · see citing works
Aizman, O., Brismar, H., Uhlén, P., Zettergren-Markus, E., Levey, A. I., Forssberg, H., Greengard, P., & Aperia, A. C. (2000) · Nature Neuroscience · doi:10.1038/72929 · Cited by 415 · see citing works
The house mouse. Development and normal stages from fertilization to 4 weeks of age.
Theiler, K. (1972) · Springer eBooks · Cited by 412 · see citing works
The origin and migration of cortical neurones: new vistas
Parnavelas, J. G. (2000) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01553-8 · Cited by 393 · see citing works
Cytoskeletal coordination during neuronal migration
Schaar, B. T., & McConnell, S. K. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506008102 · Cited by 364 · see citing works
Control of cortical interneuron migration by neurotrophins and PI3-kinase signaling
Polleux, F., Whitford, K. L., Dijkhuizen, P. A., Vitalis, T., & Ghosh, A. (2002) · Development · doi:10.1242/dev.129.13.3147 · Cited by 361 · see citing works
Shu, T., Ayala, R., Nguyen, M.-D., Xie, Z., Gleeson, J. G., & Tsai, L. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.030 · Cited by 361 · see citing works
Bellion, A. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1030-05.2005 · Cited by 354 · see citing works
Disruption in the Inhibitory Architecture of the Cell Minicolumn: Implications for Autisim
Casanova, M. F., Buxhoeveden, D. P., & Gomez, J. (2003) · The Neuroscientist · doi:10.1177/1073858403253552 · Cited by 337 · see citing works
Levitt, P. R., Eagleson, K. L., & Powell, E. M. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.05.008 · Cited by 331 · see citing works
Powell, E. M., Mars, W. M., & Levitt, P. (2001) · Neuron · doi:10.1016/s0896-6273(01)00264-1 · Cited by 321 · see citing works
Four-Dimensional Migratory Coordinates of GABAergic Interneurons in the Developing Mouse Cortex
Ang, E. S. B. C., Haydar, T. F., Gluncic, V., & Rakic, P. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-13-05805.2003 · Cited by 282 · see citing works
Generating diversity at GAB Aergic synapses
Cherubini, E. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01724-0 · Cited by 257 · see citing works
Zhu, Y., Li, H.-S., Zhou, L., Wu, J. Y., & Rao, Y. (1999) · Neuron · doi:10.1016/s0896-6273(00)80801-6 · Cited by 243 · see citing works
Ventricle-directed migration in the developing cerebral cortex
Nadarajah, B., Alifragis, P., Wong, R., & Parnavelas, J. G. (2002) · Nature Neuroscience · doi:10.1038/nn813 · Cited by 219 · see citing works
Dopamine Modulates Cell Cycle in the Lateral Ganglionic Eminence
Ohtani, N., Goto, T., Waeber, C., & Bhide, P. G. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-07-02840.2003 · Cited by 193 · cited 10× · see citing works
“A likely explanation for D1 receptor-like effects of dopamine is that the density of D1 receptor binding sites is 10-fold higher than D2 receptor binding sites in the E15 mouse striatum (Ohtani et al., 2003).”
BackgroundMethodInfluentialSelf-citationMorris, N. R. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.148.6.1097 · Cited by 177 · see citing works
LIS1 and dynein motor function in neuronal migration and developmentPreprint
Wynshaw-Boris, A. J., & Gambello, M. J. (2001) · Genes & Development · doi:10.1101/gad.886801 · Cited by 166 · see citing works
Interneurons set the tune of developing networks
Ben‐Ari, Y., Khalilov, I., Represa, A., & GOZLAN, H. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.05.002 · Cited by 149 · see citing works
Morris, S. M., Albrecht, U., Reiner, O., et al. (1998) · Current Biology · doi:10.1016/s0960-9822(98)70232-5 · Cited by 149 · see citing works
Yozu, M., Tabata, H., & Nakajima, K. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2072-05.2005 · Cited by 144 · see citing works
Alifragis, P., Liapi, A., & Parnavelas, J. G. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1245-04.2004 · Cited by 143 · see citing works
Genetic Control of Cortical Development
Rubenstein, J. L. R. (1999) · Cerebral Cortex · doi:10.1093/cercor/9.6.521 · Cited by 141 · see citing works
Krimer, L. S., & Goldman-Rakic, P. S. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-11-03788.2001 · Cited by 141 · see citing works
Popolo, M., McCarthy, D. M., & Bhide, P. G. (2004) · Developmental Neuroscience · doi:10.1159/000082140 · Cited by 113 · see citing works
Self-citationWang, H. Y., Runyan, S., Yadin, E., & Friedman, E. (1995) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)09613-2 · Cited by 105 · see citing works
Jung, A. B., & Bennett, J. P. (1996) · Developmental Brain Research · doi:10.1016/0165-3806(96)00033-8 · Cited by 94 · see citing works
Robinson, P. D., Schutz, C. K., Macciardi, F. M., White, B. N., & Holden, J. J. A. (2001) · American Journal of Medical Genetics · doi:10.1002/ajmg.1187 · Cited by 88 · see citing works
Friedman, E., Yadin, E., & Wang, H. Y. (1996) · Neuroscience · doi:10.1016/s0306-4522(96)83011-9 · Cited by 84 · see citing works
Crandall, J. E. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh027 · Cited by 80 · see citing works
Self-citationStanwood, G. D., & Levitt, P. R. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4591-06.2007 · Cited by 60 · see citing works
Application of quantitative RT-PCR to the analysis of dopamine receptor mRNA levels in rat striatum
Vrana, S. L., Kluttz, B. W., & Vrana, K. E. (1995) · Molecular Brain Research · doi:10.1016/0169-328x(95)00152-i · Cited by 22 · see citing works
Zhang, L., & Lidow, M. S. (2002) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(02)00104-1 · Cited by 22 · see citing works
Schama, K. F., Howell, L. L., & Byrd, L. D. (1998) · Elsevier eBooks · doi:10.1016/b978-012347360-8/50009-4 · Cited by 17 · see citing works
Characterization of Mouse Striatal Precursor Cell Lines Expressing Functional Dopamine Receptors
Araki, K. Y., Fujimura, S., MacDonald, M. E., & Bhide, P. G. (2006) · Developmental Neuroscience · doi:10.1159/000095114 · Cited by 9 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Consensus Paper: Pathological Role of the Cerebellum in Autism
Fatemi, S. H., Aldinger, K. A., Ashwood, P., Bauman, M. L., Blaha, C. D., Blatt, G. J., Chauhan, A., Chauhan, V., Dager, S. R., Dickson, P. E., et al. (2012) · The Cerebellum · doi:10.1007/s12311-012-0355-9 · Cited by 723 · see citing works
Development of prefrontal cortex
Kolk, S. M., & Rakic, P. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01137-9 · Cited by 378 · see citing works
“It has furthermore been shown that dopamine and GABA interactions can influence these processes [187, 188].”
BackgroundDevelopmental origins of brain disorders: roles for dopamine
Money, K. M., & Stanwood, G. D. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00260 · Cited by 221 · see citing works
Zhu, J., Zhang, X., Xu, Y., Spencer, T. J., Biederman, J., & Bhide, P. G. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1041-12.2012 · Cited by 125 · see citing works
Self-citationDecision making during interneuron migration in the developing cerebral cortex
Guo, J., & Anton, E. S. (2014) · Trends in Cell Biology · doi:10.1016/j.tcb.2013.12.001 · Cited by 104 · see citing works
Hyperactivity and male‐specific sleep deficits in the 16p11.2 deletion mouse model of autism
Angelakos, C. C., Watson, A. J., O'Brien, W. T., Krainock, K. S., Nickl‐Jockschat, T., & Abel, T. (2017) · Autism Research · doi:10.1002/aur.1707 · Cited by 83 · see citing works
Prenatal Drug Exposure Affects Neonatal Brain Functional Connectivity
Salzwedel, A. P., Grewen, K. M., Vachet, C., Gerig, G., Lin, W., & Gao, W. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.4333-14.2015 · Cited by 93 · see citing works
Bhide, P. G. (2009) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2009.01.006 · Cited by 60 · see citing works
Self-citationSalzwedel, A. P., Grewen, K. M., Goldman, B. D., & Gao, W. (2016) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2016.05.009 · Cited by 46 · see citing works
Cocaine exposure modulates dopamine and adenosine signaling in the fetal brain
Kubrusly, R. C. C., & Bhide, P. G. (2010) · Neuropharmacology · doi:10.1016/j.neuropharm.2009.09.007 · Cited by 40 · see citing works
Self-citationGarcia, L. P., Witteveen, J. S., Middelman, A., van Hulten, J. A., Martens, G. J. M., Homberg, J. R., & Kolk, S. M. (2019) · Molecular Neurobiology · doi:10.1007/s12035-018-1105-x · Cited by 28 · see citing works
Ghuman, J. K., & Ghuman, H. S. (2013) · Pediatric Drugs · doi:10.1007/s40272-012-0001-5 · Cited by 21 · see citing works
- Authors
- Crandall, J. E., McCarthy, D. M., Araki, K. Y., Sims, J. R., Ren, J.-Q., & Bhide, P. G.
- Affiliations
- University of Massachusetts Chan Medical School (US)
- Harvard University (US)
- Corresponding author
- Bhide, Pradeep G.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2007-04-04
- Volume
- 27
- Issue
- 14
- Pages
- 3813-3822
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2711976
- OpenAlex
- W1986105284
- Cited by
- 134
- References
- 60
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 4 · 2023: 5 · 2022: 4 · 2021: 2 · 2020: 7 · 2019: 7 · 2018: 7 · 2017: 7 · 2016: 3 · 2015: 5 · 2014: 11 · 2013: 11 · 2012: 16
- FWCI
- 3.08
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- The Journal of the American Medical Association (JAMA) Network (American Medical Association) (submittedVersion)
- Funders
- U.S. Public Health Service
- National Institute on Drug Abuse (R01DA020796, DA020796)
- National Institute of Neurological Disorders and Stroke (NS 43426, NS45776, R01NS043426, P30NS045776)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (P01HD005515, HD05515)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- dopamine D1 receptor, dopamine D2 receptor, basal forebrain, cerebral cortex, ganglionic eminence, embryonic brain development, neuronal migration, schizophrenia, developmental disorders
- MeSH terms
- Animals, Cell Movement, Cerebral Cortex, Female, gamma-Aminobutyric Acid, Male, Neurons, Pregnancy, Receptors, Dopamine, Dopamine Agents, Prosencephalon, Receptors, Dopamine D1, Receptors, Dopamine D2, Mice, Knockout, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
